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Abstract Chryseobacteriaconsists of important human pathogens that can cause a myriad of nosocomial infections. We isolated four multidrug‐resistantChryseobacteriumbacteria from activated sludge collected at domestic wastewater treatment facilities in the New York Metropolitan area. Their genomes were sequenced with Nanopore technology and used for a comprehensive resistomics comparison with 211Chryseobacteriumgenomes available in the public databases. A majority ofChryseobacteriaharbor 3 or more antibiotic resistance genes (ARGs) with the potential to confer resistance to at least two types of commonly prescribed antimicrobials. The most abundant ARGs, including β‐lactam class A (blaCGA‐1andblaCIA) and class B (blaCGB‐1andblaIND) and aminoglycoside (ranAandranB), are considered potentially intrinsic inChryseobacteria. Notably, we reported a new resistance cluster consisting of a chloramphenicol acetyltransferase genecatB11, a tetracycline resistance genetetX, and two mobile genetic elements (MGEs),IS91family transposase andXerDrecombinase. BothcatB11andtetXare statistically enriched in clinical isolates as compared to those with environmental origins. In addition, two other ARGs encoding aminoglycoside adenylyltransferase (aadS) and the small multidrug resistance pump (abeS), respectively, are found co‐located with MGEs encoding recombinases (e.g.,RecAandXerD) or transposases, suggesting their high transmissibility amongChryseobacteriaand across theBacteroidotaphylum, particularly those with high pathogenicity. High resistance to different classes of β‐lactam, as well as other commonly used antimicrobials (i.e., kanamycin, gentamicin, and chloramphenicol), was confirmed and assessed using our isolates to determine their minimum inhibitory concentrations. Collectively, though the majority of ARGs inChryseobacteriaare intrinsic, the discovery of a new resistance cluster and the co‐existence of several ARGs and MGEs corroborate interspecies and intergenera transfer, which may accelerate their dissemination in clinical environments and complicate efforts to combat bacterial infections.